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ARTICLE DOI: 10.1038/s42003-018-0197-1 OPEN Slow recovery from a disease epidemic in the spotted hyena, a keystone social carnivore Sarah Benhaiem 1, Lucile Marescot 1,2, Marion L. East 1, Stephanie Kramer-Schadt 1,3, Olivier Gimenez 2, Jean-Dominique Lebreton 2 & Heribert Hofer 1,4,5 1234567890():,; Predicting the impact of disease epidemics on wildlife populations is one of the twenty-first century’s main conservation challenges. The long-term demographic responses of wildlife populations to epidemics and the life history and social traits modulating these responses are generally unknown, particularly for K-selected social species. Here we develop a stage- structured matrix population model to provide a long-term projection of demographic responses by a keystone social predator, the spotted hyena, to a virulent epidemic of canine distemper virus (CDV) in the Serengeti ecosystem in 1993/1994 and predict the recovery time for the population following the epidemic. Using two decades of longitudinal data from 625 known hyenas, we demonstrate that although the reduction in population size was moderate, i.e., the population showed high ecological ‘resistance’ to the novel CDV genotype present, recovery was slow. Interestingly, high-ranking females accelerated the population’s recovery, thereby lessening the impact of the epidemic on the population. 1 Department of Ecological Dynamics, Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Strasse 17, D-10315 Berlin, Germany. 2 CEFE, CNRS, University Montpellier, University Paul Valéry Montpellier 3, EPHE, IRD, Montpellier 34090, France. 3 Department of Ecology, Technische Universität Berlin, Rothenburgstr. 12, 12165 Berlin, Germany. 4 Department of Veterinary Medicine, Freie Universität Berlin, Oertzenweg 19b, Berlin 14163, Germany. 5 Department of Biology, Chemistry, Pharmacy, Freie Universität Berlin, Takustr. 3, Berlin 14195, Germany. These authors contributed equally: Sarah Benhaiem, Lucile Marescot. These authors jointly supervised this work: Jean-Dominique Lebreton, Heribert Hofer. Correspondence and requests for materials should be addressed to S.B. (email: [email protected]) COMMUNICATIONS BIOLOGY | (2018) 1:201 | DOI: 10.1038/s42003-018-0197-1 | www.nature.com/commsbio 1 ARTICLE COMMUNICATIONS BIOLOGY | DOI: 10.1038/s42003-018-0197-1 pidemics responsible for a decline in keystone species can performance, social status and infection state drive both R0 and Ealter ecosystem dynamics and diminish biodiversity by the population response to a major epidemic. increasing the chance of extirpation of host populations, 1–4 and possibly the extinction of species . Human activities rapidly Results expand the geographical range and host species spectrum of Demographic, social and infection parameter estimates. Each pathogens, and epidemics caused by exotic pathogens in unex- 5 year, each female was assigned a demographic (cub, subadult, pected hosts are increasing . Viruses are of particular concern as adult breeder or adult non-breeder), a social (high or low social they evolve rapidly, yielding new strains and adaptations to novel 3,5 status) and an infection (susceptible, infected or recovered) state. hosts . We fitted a multi-event CMR (MECMR) model that accounted We know little about the long-term demographic responses to for uncertainty on the assignment of infection states, i.e., we infectious viral disease epidemics in wildlife species, particularly included animals with unknown infection states10. We focused on those with high maternal investment in a low number of offspring three periods: pre-epidemic (pre-epidem; 1990–1992), epidemic during a long lifespan (K-selected species), probably because – 6 (epidem; 1993 1994), and post-epidemic (post-epidem; longitudinal studies on such species are rare . To characterise 1995–1999). The virulent CDV strain was not detected in any of these demographic responses, we apply two terms from the field 10 — our study clans after 1997 and it was not detected in any host in of ecology ecological resistance: the impact of exogenous dis- the Serengeti ecosystem after 199919. turbance on the state of a system; and recovery: the endogenous The annual apparent survival probability (ϕ) varied over time, process that pulls the disturbed system back towards equili- being highest during pre-epidem and lowest during epidem for brium7. In social host species, the relationships between social 8–10 all states, as the effect of periods was additive to the effect of traits and disease outcomes can be complex . It is therefore given states (Table 1). The transition probability from the unclear how social traits modulate the magnitude of the potential susceptible to the infected state (β, the infection probability) also reduction in host population size during an epidemic, or the 11 varied across periods; it was highest during epidem and lowest recovery time to pre-epidemic population size . during pre-epidem. CDV infection requires contact with aerosol There is a strong need for a robust predictive framework to droplets and body fluids from virus shedding individuals20. assess the potential risk that epidemics pose to wildlife popula- High-ranking subadults, breeders and non-breeders had a higher tions, to provide projections of the recovery of populations from infection probability than low-ranking ones (Table 1), a epidemics and to identify factors modulating population consequence of their higher contact rates10,21. As described responses, particularly for K-selected and social species. Here we 10,20 12,13 previously , CDV infection decreased survival only among show that stage-structured matrix population models are cubs and subadults but not adults (whether breeders or non- highly suitable for these purposes because they allow us to assess breeders, Table 1). Cubs of low-ranking mothers had a higher how demographic performance (in terms of fecundity, survival fl infection probability and were less likely to survive CDV and reproductive value) is in uenced by infection status, and how infection than those of high-ranking mothers. This is thought disease persistence and dynamics are influenced by host demo- 14,15 to be a consequence of their poorer body condition and lower graphy and social structure . Such models can make full use of allocation of resources to immune processes10. High-ranking field data as input, i.e., state-specific parameters estimated by ψ 16 females were more likely to become breeders ( , the probability capture-mark-recapture (CMR) approaches , and permit the of assuming a breeder state) than low-ranking females. High- calculation of the basic reproduction number (R0)ofa 14,15 ranking females were less likely than low-ranking ones to pathogen . R0 is a measure of the number of individuals maintain their social status (r, the probability of maintaining the infected by introducing a single infected individual into a sus- 17 current social state). Estimates of all parameters for each period, ceptible population (over the course of its infectious period) , which were used as input for the subsequent stage-structured i.e., a measure of maximum transmissibility, and describes whe- matrix population model, are shown in Table 1. Probabilities of ther an infectious disease will invade or fade out in a population. detection and assignment of infection states were assumed to be Here, we applied a stage-structured matrix population model constant throughout the study period. to a longitudinal dataset of 625 individually known female spotted hyenas Crocuta crocuta (hereafter hyenas) in the Seren- Population and CDV dynamics. The population growth rate (λ) geti National Park, Tanzania, spanning two decades. We inves- λ tigated the population consequences of a canine distemper virus differed substantially between periods (Fig. 1). was highest (CDV) epidemic10,18, caused by a novel genotype better adapted during pre-epidem and lowest during epidem. The hyena popu- to non-canids such as hyenas and lions Panthera leo than to lation increased during pre-epidem but decreased during epidem canids19. By quantifying and conducting a sensitivity analysis for and post-epidem (Fig. 1). fi We estimated CDV R0 in a closed hyena population, based on R0 of this CDV strain for the rst time in hyenas, we formally demonstrate that it was highly contagious among hyenas during our three study clans, and hence did not consider the spread of fl the non-canid strain in other non-canid species, such as the lion, the epidemic and that the most in uential parameter to decrease 19 R was the probability of becoming a socially high-ranking which were infected with this strain during the epidemic .We 0 modified a previously developed approach for discrete time breeder. CDV infection during the epidemic decreased the sur- 14,15 vival of cubs and subadults, particularly low-ranking ones. The models . Incorporating population growth rate into the projected hyena population showed a slow recovery, taking at calculation produced a measure of change in the rate of spread least 16 years to return to pre-epidemic levels. Population growth of the disease accounting for change in population size, i.e., measuring change in the incidence rate of the disease. We then rate and R0 were particularly sensitive to changes in the demo- fi graphic contribution of high-ranking females, in terms of their estimated this modi ed version of R0 during the epidemic period. probabilities of recruitment, survival and maintenance of high R0 was relatively high, equal to 5.69 ± 0.67, illustrating